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Evolution in Structured Populations

Multilevel Selection On Mating Success In Water Striders

In the past several weeks I have been discussing how multilevel selection was very common in plants. Of course, we should not be surprised that multilevel selection would be important in plants, since they are sessile, and often have limited gene flows. Thus, they are forced to interact with a consistent set of partners, and the population viscosity will lend heritability to many contextual traits. Animals have much fewer constraints on their interactions, thus we might expect group selection to be rarer in animals than plants. I am not sure if I believe that or not. All of the original theorizing around group selection was about animals, and plants because they didn’t “behave” were essentially never discussed. Indeed, Herron and Freeman’s Evolutionary Analysis uses my thesis on Arabidopsis to point out that group selection isn’t just in animals. So my early training tends to make me assume that group selection is more important in animals than plants.

Be that as it may, it is worth looking at a contextual analysis experiment in animals. The study I want to talk about is Eldakar, Wilson, Dlugos, and Pepper (2010, Evolution64, 3183). This study is also interesting in that it uses contextual analysis in a manipulated experimental setup. In this study Eldakar and colleagues set up a large pool (basically a child’s wading pool) with partial partitions and a current running around the outer rim of the pool. I have looked around the web for a picture, but I couldn’t find one (Omar: We need pictures!), so based on my reading of their paper this is what it looked like.

Schematic of experimental pools used by Eldakar et al. The pools were 3 meters in diameter, and had six sub pools with a current flowing around the outside edge.

Water striders were added to this experimental metapopulation and allowed to interact, and mate. This was a typical behavioral experiment in that the different water striders were individually identified, and at regular intervals their behaviors were scored. The water striders were given 10 days to settle in, and initial observations were made, and then a further 10 days in which data were gathered.

It is important to spend a little time commenting on water strider behavior (of which I know very little). In particular, as with many animals there is strong sexual selection, which means that the females are continually harassed, and males are more or less constantly trying to mate with them. As you might expect the females don’t particularly appreciate (or need) all of this attention, so generally speaking females spend a lot of time avoiding having to copulate with males. On the other hand males can be ranked for aggressiveness. Eldakar and his colleagues identified a series of mating related behaviors, and using the frequency of these behaviors classified the males as to degree of aggressiveness. As you might expect, in a confined space very aggressive males get more matings than less aggressive males, however, when females have a choice in the matter they are inclined to run away from these hyper-aggressive males.

So with that in mind the water striders were placed in the pool and allowed to move wherever they wanted. Naturally the assorted into the six quiet sub pools, but they were able to use the current along the edge to move from sub pool to sub pool. From this an interesting thing happened. That is females tended to leave sub pools with a lot of aggressive males, and congregate in pools with more docile males:

“Figure 1: Individual dispersal in response to local aggression imposes sex-ratio heterogeneity among subpools. The frequency of females within subpools decreased as the average aggression score within subpools increased.” (from Eldakar, Wilson, Dlugos, and Pepper. 2010, Evolution64, 3183).

What this means is that the very aggressive males got fewer matings, because although they were more successful at obtaining matings, because of their aggressiveness and female movement they had less access to females than did less aggressive males. In short, the highest mating success was found in males with an intermediate level of aggression.

They used contextual analysis to estimate the strengths of selection on individual aggressiveness and selection on group mean aggressiveness. In this they found that there was strong individual selection favoring more aggressive males (slope of regression of relative fitness on individual aggressiveness score = strength and direction of individual selection = 0.752, P=0.019), and group selection favoring decreased average aggressiveness (slope of regression of relative fitness on group mean aggressiveness score = strength and direction of group selection = – 0.556, P=0.076). The group selection regression coefficient is not significant (probably due to the lower power and smaller degrees of freedom at the group level), nevertheless, it is certainly having an effect on the outcome, so this is a place were it seems to me that special pleading is justified.

That this was indeed to female movement can be seen from two observations. First, less aggressive males tended to be near females more often than highly aggressive males:

Second, in an earlier paper (Eldakar, Dlugos, Pepper, and Wilson 2009. Science326, 816.) they showed that limiting the dispersal of females qualitatively changed the relationship between aggression and mating success in the males, with more aggressive males always getting more matings.

As I advocated for last week, this study uses contextual analysis to measure the strength of selection, and to form the hypothesis that group selection against aggressiveness is acting through female dispersal. However, it is the additional observations on the behavior of females, and manipulations of their ability to emigrate that confirm that the group selection is mediated by dispersal of females.

Another interesting point is that if we assume that aggressiveness is at its multilevel selected optimum, and make the probably silly assumption that the traits at the two levels are uncorrelated, we can actually estimate the ratio of the heritability of the group level trait to the individual level trait. As I discussed earlier, using Goodnight (2005 Population Ecology47, 3) and assuming that selection is in equilibrium, with no correlated responses to selection, then we can re-write Hamilton’s rule as:

In other words, accepting all of my sketchy assumptions, this suggests that the heritability of the group trait of mean aggressiveness has a heritability that is a third greater than the heritability at the individual level. This might not be unreasonable given that interactions among individuals (males scaring off females) can contribute to the group heritability, but not the individual heritability.

In any case I have over-extended by stay on this weeks post, so suffice it to say that I suspect that sexual selection may be a ripe place to look for group selection in animals.

What a neat study. Mating behavior is a great venue for studying multilevel selection.

Back in the early ’90s I had a proposal to use fruit fly mating speed as an experimental group character, because it’s a joint property of the male and female. Like water striders, females get harassed by aggressive males, and the large legacy of D. melanogaster mating speed experiments offers a multitude of potential contextual traits to consider. My goal was to pair the MLS fitness analysis with an explicit quantitative genetic analysis. Since D. melanogaster only has four chromosomes, the “group” (male+female) only has eight. This affords an opportunity to estimate things like cross-gender dominance and epistasis, etc.